Facultative cleaning of spiral‐horned antelope by the African paradise flycatcher (Terpsiphone viridis)

Abstract In cleaning associations, individuals known as “cleaners” remove and feed on parasites and pests found on, or around, other animals known as “clients.” While best documented in marine environments and as mutualisms, cleaning associations are widespread in terrestrial systems and range along a spectrum of obligate to facultative associations. In African savannas, cleaning associations primarily comprise facultative interactions between mammals and birds that remove attached parasites. Few reports, however, exist on cleaning associations that involve the removal of unattached pests. In this short note, I report a novel facultative bird–ungulate cleaning association involving the removal of unattached pests, between the African paradise flycatcher (Terpsiphone viridis) and two species of spiral‐horned antelope (Tragelaphus spp.): greater kudu (Tragelaphus strepsiceros) and Cape bushbuck (Tragelaphus sylvaticus). On multiple occasions, I observed African paradise flycatchers hawking flying insects around greater kudu and a Cape bushbuck during the dry season at the Mpala Research Centre in Laikipia, Kenya. These observations document a rare feeding strategy for the African paradise flycatcher and are among the few records on cleaning interactions involving the removal of unattached pests.

the direct removal of ticks and other attached parasites that they are unable to reach or detach themselves, but they may also benefit from the removal of unattached pests (e.g., insects) that swarm around them or fly into mucous membranes (Palmer et al., 2019).
In terrestrial systems, cleaning associations are dominated by interactions between birds and mammals, a large majority of which are facultative and are reported to occur in Africa (Dean & MacDonald, 1981;Nyaguthii et al., 2021;Sazima, 2011). Cleaner birds in these systems often employ one of two strategies: (1) "gleaning," which involves the removal of attached parasites by perching on the backs of mammal clients, or (2) "hawking," which involves the removal of unattached pests by feeding on the wing and returning to a perching site (Dean & MacDonald, 1981;Sazima, 2011). Well-known examples of African facultative mammal gleaners include red-and pale-winged starlings (Fennessy, 2003;Penzhorn & Horak, 1989), yellow-bellied bulbuls (Roberts, 1993), African jacanas (Ruggiero, 2008), and others (Dean & MacDonald, 1981;Nyaguthii et al., 2021) that clean ticks and other arthropods. By contrast, few instances of facultative hawkers of insects attracted to wildlife (i.e., unattached pests) exist.
Here, I report a series of novel observations of the African paradise flycatcher (Passeriformes: Monarchidae, Terpsiphone viridis) hawking insects around greater kudu (Tragelaphus strepsiceros) and Cape bushbuck (Tragelaphus scriptus). With the exception of one reported interaction with a red duiker in False Bay Park, South Africa (Dean & MacDonald, 1981), African paradise flycatchers have not previously been documented to forage on insects attracted to wild ungulates. These observations, therefore, document an unusual feeding strategy for the African paradise flycatcher and contribute to a growing body of literature on facultative cleaning associations between birds and ungulates in African savannas.

| Species
The African paradise flycatcher is an insectivorous species of passerine bird found across sub-Saharan Africa, most recognized for its striking appearance. Individuals occur in white and rufous color morphs with males exhibiting long central tail feathers that extend into streamers. To capture insects, African paradise flycatchers employ various feeding strategies, the most common being hawking insects from the air or gleaning them from branches and the undersides of leaves (Branfield, 2012;Fraser, 1983). Tragelaphine antelopes, including Cape bushbuck and greater kudu, are broadly distributed across sub-Saharan Africa, often in forest or thicket habitats where they browse on woody plants (Khademi, 2017). MRC is a ~ 20,000 ha ranch and wildlife conservancy comprising semi-arid thorn-scrub savanna that hosts a great diversity of avian and ungulate wildlife along with domestic cattle, camel, sheep, goat, and donkey (Kartzinel et al., 2019;Young et al., 1997). Both wild and domestic ungulates frequent the field station at the southern end of the property, which is fenced to exclude elephants and accordingly supports dense woody vegetation. Greater kudu typically forage in mixed-sex groups of 2-5 individuals consisting of adult females, juveniles, and young adult males, while Cape bushbuck forage solitarily. Both species often attract high densities of insects that swarm around them (Figure 1).

| RE SULTS
From March 13 to 25, 2022, I observed six cleaning interactions between African paradise flycatchers and greater kudu and one with a lone Cape bushbuck (Table 1, see Video S1). All observed interactions took place during a prolonged dry season in a below-average rainfall year at MRC (Caylor et al., 2019), between 12 p.m. and 6 p.m. Among the multiple feeding strategies that African paradise flycatchers employ to capture invertebrate prey, associating with and hawking insects around wildlife appears to be rare. Only one record on such an association with a red duiker exists (Dean & MacDonald, 1981). The seven cleaning interactions that I observed over the span of 11 days are therefore peculiar and raise the question as to whether such interactions are more common during periods of low insect activity or abundance such as in the dry season and whether such cleaning behaviors have become established in the African paradise flycatcher population at MRC. As no further efforts were made to document these interactions over time, future cross-seasonal comparisons may provide insight into the broader role that African paradise flycatchers may play as cleaners of African ungulates.
Additionally, it is important to note that these observations took place within the confines of a fenced research center. Numerous reports on cleaning associations between birds and ungulates come from areas of recreation and conservation (D'Angelo et al., 2016;Gijsman & Guevara, 2020), including a recent observation of a black-cheeked waxbill (Brunhilda charmosyna) cleaning a Kirk's dikdik (Madoqua kirkii), also during the dry season at MRC (Nyaguthii et al., 2021). Two hypotheses could potentially explain this pattern.
First, recreation and conservation areas may provide researchers with more opportunities to interact with wildlife and thus easily record associations that would otherwise be hard to observe in more remote natural areas (Lopez et al., 2020). Second, recreation or human-frequented areas may also indirectly promote novel species interactions by attracting species seeking anthropogenic food subsidies (Birnie-Gauvin et al., 2017;Marzluff, 2001) or spatial refugia from predators (Leighton et al., 2010;Muhly et al., 2011;Suraci et al., 2019). For instance, greater kudu and Cape bushbuck regularly visit MRC to forage within its protective enclosure and often do so with remarkably predictable foraging routes and patterns (FG, pers.  (Dean & MacDonald, 1981).
Lastly, as greater kudu and Cape bushbuck often attract large swarms of insects and are important blood meal sources for biting insects like tsetse flies across much of their ranges (Gaithuma et al., 2020;Moloo, 1993), such associations can be beneficial if they substantially reduce the prevalence and abundance of diseasecarrying insects flying around them. Analogously, by associating with ungulates swarmed by insects, African paradise flycatchers may benefit from a reduction in prey search time and increase their likelihood of finding food. Whether the benefits accrued by both partners through these interactions are considerable, however, is unknown and would depend on the number and types of insects that were removed by flycatchers from the airspace around the ungulates -both of which I was unable to ascertain through these observations. Further investigations may elucidate whether these types of associations are frequent occurrences and a common feeding strategy for African paradise flycatchers and other cleaning birds.

ACK N OWLED G M ENTS
I thank the Mpala Research Centre for hosting me during the period over which these interactions were observed. I also thank Robert M. Pringle and Alexander Jacobsen for providing feedback on an earlier draft. Finally, I thank Damien Farine and another anonymous reviewer for taking the time and effort necessary to review this manuscript. Funding for this research and fieldwork was provided by the

Mohamed bin Zayed Species Conservation Fund and the Princeton
Institute for International and Regional Studies. Data for this project were collected under the research permit NACOSTI/P/21/8819 from the Kenya National Commission for Science, Technology, and Innovation. This publication was supported by the Princeton University Library Open Access Fund.

CO N FLI C T O F I NTE R E S T
The author also declares no conflict of interest.

DATA AVA I L A B I L I T Y S TAT E M E N T
Data collected for this project are available in Table 1 of this manuscript.